Orbitofrontal neurons acquire responses to ‘valueless’ Pavlovian cues during unblocking

McDannald, Michael A.; Esber, Guillem R.; Wegener, Meredyth A; Wied, Heather M.; Liu, Tzu Lan; Stalnaker, Thomas A.; Jones, Joe M.; Trageser, Jason C.; Schoenbaum, Geoffrey

doi:10.7554/elife.02653

Cited by 68 publications

(72 citation statements)

References 34 publications

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“…This requires the ability to predict what specific outcomes are available in the environment and the ability to use that information to retrieve those outcomes' current values to guide behavior (Pickens et al, 2003;West et al, 2011;Jones et al, 2012). Although general or abstract value correlates have been prominently reported in lateral OFC (lOFC) (Padoa-Schioppa andAssad, 2006, 2008;Padoa-Schioppa, 2009, 2013, they are arguably more often identified in medial OFC (mOFC) (Plassmann et al, 2007(Plassmann et al, , 2010Hare et al, 2008Hare et al, , 2010Levy and Glimcher, 2011;McNamee et al, 2013;Strait et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Across two experiments, we recorded neurons in the lOFC in rats learning about cues that signaled changes in an expected outcome. In the first study (McDannald et al, 2014), we compared firing to cues that signaled either a shift in reward flavor or shift in reward value. To our surprise, we found similar representation of these two cues, even though one reflected a valueless change in reward features.…”

Section: Introductionmentioning

confidence: 99%

“…This result was more consistent with a feature representation than with a representation tied to value. To explore this further, we conducted a second study (Lopatina et al, 2015), in which we compared firing in lOFC neurons to cues that signaled more reward, less reward, or no change in reward. Despite the linear change in value across cues, a change reflected in the rats' behavior, we failed to find neural correlates that reflected reward value across cues.…”

Section: Introductionmentioning

confidence: 99%

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Medial Orbitofrontal Neurons Preferentially Signal Cues Predicting Changes in Reward during Unblocking

Lopatina

McDannald

Styer

et al. 2016

Journal of Neuroscience

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The orbitofrontal cortex (OFC) has been broadly implicated in the ability to use the current value of expected outcomes to guide behavior. Although value correlates have been prominently reported in lateral OFC, they are more often associated with more medial areas. Further, recent studies in primates have suggested a dissociation in which the lateral OFC is involved in credit assignment and representation of reward identity and more medial areas are critical to representing value. Previously, we used unblocking to test more specifically what information about outcomes is represented by OFC neurons in rats; consistent with the proposed dichotomy between the lateral and medial OFC, we found relatively little linear value coding in the lateral OFC (Lopatina et al., 2015). Here we have repeated this experiment, recording in the medial OFC, to test whether such value signals might be found there. Neurons were recorded in an unblocking task as rats learned about cues that signaled either more, less, or the same amount of reward. We found that medial OFC neurons acquired responses to these cues; however, these responses did not signal different reward values across cues. Surprisingly, we found that cells developed responses to cues predicting a change, particularly a decrease, in reward value. This is consistent with a special role for medial OFC in representing current value to support devaluation/revaluation sensitive changes in behavior.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Medial Orbitofrontal Neurons Preferentially Signal Cues Predicting Changes in Reward during Unblocking

Lopatina

McDannald

Styer

et al. 2016

Journal of Neuroscience

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“…The orbitofrontal portion of the prefrontal cortex (OFC) in particular has been found to have a role in decisions based on outcome value and reward expectations (Kepecs et al, 2008;McDannald et al, 2014;Padoa-Schioppa and Cai, 2011;Stalnaker et al, 2014). When rewards are uncertain, the magnitude of response in OFC has been shown to modulate proportionally with risk (Tobler et al, 2009), and lesions of OFC disrupt decisions that involve risk (Hsu et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Consequences of Adolescent Ethanol Consumption on Risk Preference and Orbitofrontal Cortex Encoding of Reward

McMurray

Amodeo

Roitman

2015

Neuropsychopharmacol

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Critical development of the prefrontal cortex occurs during adolescence, a period of increased independence marked by decision making that often includes engagement in risky behaviors, such as substance use. Consumption of alcohol during adolescence has been associated with increased impulsivity that persists across the lifespan, an effect which may be caused by long-term disruptions in cortical processing of rewards. To determine if alcohol consumption alters cortical encoding of rewards of different sizes and probabilities, we gave rats limited access to alcohol in gelatin during adolescence only. In adulthood, we recorded the electrophysiological activity of individual neurons of the orbitofrontal cortex while rats performed a risk task that varied the level of risk from day-to-day. Rats that had consumed higher levels of alcohol showed increased risk preference in the task compared with control and low alcohol-consuming rats. Patterns of neuronal responses were identified using principal component analysis. Of the multiple patterns observed, only one was modulated by adolescent alcohol consumption and showed strongest modulation after reward receipt. This subpopulation of neurons showed blunted firing rates following rewards in alcohol-consuming rats, suggesting a mechanism through which adolescent alcohol exposure may have lasting effects on reward processing in the context of decision making. The differences in OFC responses between high alcohol consumers and control animals not given access to alcohol support the idea that, regardless of potential variability in innate alcohol preferences, voluntary consumption of alcohol during adolescence biases choice patterns longitudinally through alterations in cortical function.

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“…are necessary. Recent data suggest that the OFC is involved in signaling information about specific outcomes (9)(10)(11)(12)(13)(14). For instance, many OFC neurons signal both the value and the identity of the predicted outcome (12), and OFC lesions diminish the effects of outcome identity (but not general affective value) on conditioned behavior (13).…”

mentioning

confidence: 99%

Identity-specific coding of future rewards in the human orbitofrontal cortex

Howard

Gottfried

Tobler

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

192

180

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Nervous systems must encode information about the identity of expected outcomes to make adaptive decisions. However, the neural mechanisms underlying identity-specific value signaling remain poorly understood. By manipulating the value and identity of appetizing food odors in a pattern-based imaging paradigm of human classical conditioning, we were able to identify dissociable predictive representations of identity-specific reward in orbitofrontal cortex (OFC) and identity-general reward in ventromedial prefrontal cortex (vmPFC). Reward-related functional coupling between OFC and olfactory (piriform) cortex and between vmPFC and amygdala revealed parallel pathways that support identityspecific and -general predictive signaling. The demonstration of identity-specific value representations in OFC highlights a role for this region in model-based behavior and reveals mechanisms by which appetitive behavior can go awry.reward value | associative learning | ventromedial prefrontal cortex | olfaction | multivoxel pattern analysis P redictive representations of future outcomes are critical for guiding adaptive behavior. To choose different types of rewards, such as food, shelter, and mates, it is essential that predictive signals contain specific information about the identity of those outcomes. Food rewards differ dramatically in their nutritional composition, and identity-specific cues allow differential foraging depending on current needs of the organism. The absence of precise mappings between predictive reward signals and their intended outcomes would have devastating effects on foodbased decisions.Despite the ecological relevance of outcome-specific predictive coding, which can be observed even in Drosophila (1), most research in human and nonhuman primates has focused on "common currency" signals of economic values in the orbitofrontal cortex (OFC) (2, 3) and ventromedial prefrontal cortex (vmPFC) (4-8). These signals, which by definition are independent of the specific nature of the reward, can be used to compare and choose between alternative outcomes, but are unable to inform expectations about the specific identity of the outcome. For this, identity-specific representations that conjointly represent information about both affective value (how good is it?) and outcome identity (what is it?) are necessary. Recent data suggest that the OFC is involved in signaling information about specific outcomes (9-14). For instance, many OFC neurons signal both the value and the identity of the predicted outcome (12), and OFC lesions diminish the effects of outcome identity (but not general affective value) on conditioned behavior (13).Recent imaging work has also begun to address how the human brain encodes predictive information about rewarding outcomes. One study (9) used a functional magnetic resonance imaging (fMRI) adaptation paradigm to provide evidence for identity-based codes for reward in the OFC. Another investigation (4) used fMRI data from a willingness to pay auction combined with decoding techniques to reveal...

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Orbitofrontal neurons acquire responses to ‘valueless’ Pavlovian cues during unblocking

Cited by 68 publications

References 34 publications

Medial Orbitofrontal Neurons Preferentially Signal Cues Predicting Changes in Reward during Unblocking

Medial Orbitofrontal Neurons Preferentially Signal Cues Predicting Changes in Reward during Unblocking

Consequences of Adolescent Ethanol Consumption on Risk Preference and Orbitofrontal Cortex Encoding of Reward

Identity-specific coding of future rewards in the human orbitofrontal cortex

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